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Viruses, Fungi and Plants: Cross-Kingdom Communication and Mutualism

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Biocommunication of Fungi

Abstract

Plants in natural ecosystems are symbiotic with fungal endophytes that have profound effects on host ecophysiology. In addition, symbiotic fungi may contain viruses that influence fungal physiology and alter the outcome of plant–fungal symbioses. For example, Dichanthelium lanuginosum is a plant that thrives in geothermal soils, tolerating root zone temperatures up to 60°C. Thermotolerance is dependent on the fungal endophyte Curvularia protuberata. Remarkably, the ability of C. protuberata to confer heat tolerance requires a double stranded RNA virus harbored by the fungus. When C. protuberata (containing the virus) and D. lanuginosum are grown independent of each other, they only tolerate temperatures up to 38°C. This is a clear example of how a symbiosis achieves something that the individual components cannot. In this chapter, we describe how this three-way symbiosis allows three organisms to survive in an environment they cannot tolerate on their own and explain what is known about the inter-organismal communication responsible for this mutualism.

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References

  • Allen TD, Dawe AL, Nuss DL (2003) Use of cDNA microarrays to monitor transcriptional responses of the chestnut blight fungs Cryphonectria parasitica to infection by virulence-attenuating hypoviruses. Eukaryot Cell 2:1253–1265

    Article  PubMed  CAS  Google Scholar 

  • de Bary A (1879) Die Erschenung Symbiose. In: Trubner KJ (ed) Vortrag auf der Versammlung der Naturforscher und Artze zu Cassel, pp 1–30

    Google Scholar 

  • Deng F, Allen TD, Hillman BI, Nuss DL (2007) Comparative analysis of alterations in host phenotype and transcript accumulation following hypovirus and mycoreovirus infections of the chestnut blight fungus Cryphonectria parasitica. Eukaryot Cell 6:1286–1298

    Article  PubMed  CAS  Google Scholar 

  • Finlay BJ, Esteban GF (2009) Can biological complexity be rationalized? Bioscience 59:333–340

    Article  Google Scholar 

  • Ghabrial SA, Suzuki N (2008) Fungal viruses. In: Granoff A, Webster R (eds) Encyclopedia of virology. Elsevier, Amsterdam, pp 284–291

    Chapter  Google Scholar 

  • Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384

    Article  PubMed  CAS  Google Scholar 

  • Hirsch AM (2004) Plant-microbe symbioses: a continuum from commensalism to parasitism. Symbiosis 37:345–363

    CAS  Google Scholar 

  • Knauth LP, Kennedy MJ (2001) The late Precambrian greening of the Earth. Nature 460:728–732

    Google Scholar 

  • Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ (2007) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol 174:648–657

    Article  PubMed  Google Scholar 

  • Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant – three way symbiosis required for thermal tolerance. Science 315:513–515

    Article  PubMed  Google Scholar 

  • Miglia KJ, McArthur ED, Redman RS, Rodriguez RJ, Zak JC, Freeman DC (2007) Genotype, soil type, and locale effects on reciprocal transplant vigor, endophyte growth, and microbial functional diversity of a narrow sagebrush hybrid zone in Salt Creek, Canyon, Utah. Am J Bot 94:425–436

    Article  PubMed  Google Scholar 

  • Milgroom MG, Cortesi P (2004) Biological control of chestnut blight with hypovirulence: a critical analysis. Annu Rev Phytopathol 42:311–338

    Article  PubMed  CAS  Google Scholar 

  • Morsy MR, Oswald J, He J, Tang Y, Roossinck MJ (2010) Teasing apart a three-way symbiosis: transcriptome analyses of Curvularia protuberata in response to viral infection and heat stress. Biochem Biophys Res Commun 401:225–230

    Article  PubMed  CAS  Google Scholar 

  • Payne JL, McClain CR, Boyer AG et al (2011) The evolutionary consequences of oxygenic photosynthesis: a body size perspective. Photosynth Res 107:37–57

    Article  PubMed  CAS  Google Scholar 

  • Pearson MN, Beever RE, Boine B, Arthur K (2009) Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol Plant Pathol 10:115–128

    Article  PubMed  CAS  Google Scholar 

  • Petrini O (1986) Taxonomy of endophytic fungi of aerial plant tissues. In: Fokkema NJ, van den Heuvel J (eds) Microbiology of the phyllosphere. Cambridge University Press, Cambridge, pp 175–187

    Google Scholar 

  • Pinto-Tomas AA, Anderson MA, Suen G et al (2009) Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 326:1120–1123

    Article  PubMed  CAS  Google Scholar 

  • Pirozynski KA, Malloch DW (1975) The origin of land plants a matter of mycotrophism. Biosystems 6:153–164

    Article  PubMed  CAS  Google Scholar 

  • Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921

    Article  PubMed  CAS  Google Scholar 

  • Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis. Science 298:1581

    Article  PubMed  CAS  Google Scholar 

  • Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness and adaptation of rice plants to cold, drought and salt stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6(7):e14823. doi:10.1371/journal.pone.0014823

    Article  PubMed  CAS  Google Scholar 

  • Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez RJ, Henson J, van Volkenburgh E et al (2008) Stress tolerance in plants via habitat-adapted symbiosis. Int Soc Microb Ecol 2:404–416

    Google Scholar 

  • Rodriguez RJ, White JFJ, Arnold AE, Redman RS (2009a) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez RJ, Freeman DC, McArthur ED, Kim YO, Redman RS (2009b) Symbiotic regulation of plant growth, development and reproduction. Commun Integr Biol 2:1–3

    Article  Google Scholar 

  • Roossinck MJ (2010) Lifestyles of plant viruses. Philos Trans R Soc B 365:1899–1905

    Article  Google Scholar 

  • Roossinck MJ (2011) The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9:99–108

    Article  PubMed  CAS  Google Scholar 

  • Schmitt MJ, Breinig F (2006) Yeast viral killer toxins: lethality and self-protection. Nat Rev Microbiol 4:212–221

    Article  PubMed  CAS  Google Scholar 

  • Shang J, Wu X, Lan X et al (2008) Large-scale expressed sequence tag analysis for the chestnut blight fungus Cryphonectria parasitica. Fungal Genet Biol 45:319–327

    Article  PubMed  CAS  Google Scholar 

  • Woodward C, Hansen L, Beckwith F, Redman RS, Rodriguez RJ (2012) Symbiogenics: An epigenetic approach to mitigating impacts of climate change on plants. HortScience, In Press.

    Google Scholar 

  • Xu P, Chen F, Mannas JP, Feldman T, Sumner LW, Roossinck MJ (2008) Virus infection improves drought tolerance. New Phytol 180:911–921

    Article  PubMed  Google Scholar 

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Acknowledgements

Funding was provided by USGS, NSF (0414463&0950447), US/IS BARD (3260-01C) and ARO (54120-LS).

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Correspondence to Rusty J. Rodriguez .

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© 2012 Springer Science+Business Media Dordrecht

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Rodriguez, R.J., Roossinck, M. (2012). Viruses, Fungi and Plants: Cross-Kingdom Communication and Mutualism. In: Witzany, G. (eds) Biocommunication of Fungi. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4264-2_14

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